University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Parasitology, Harold W. Manter Laboratory of Laboratory of Parasitology

2015 Hymenolepis folkertsi n. sp. (Eucestoda: Hymenolepididae) in the Oldfield ouM se Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the Southeastern Nearctic with Comments on Tapeworm Faunal Diversity among Deer Mice Arseny A. Makarikov Russian Academy of Sciences, [email protected]

Todd N. Nims Georgia Perimeter College

Kurt E. Galbreath Northern Michigan University

Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubs Part of the Biodiversity Commons, Ecology and Evolutionary Biology Commons, Parasitology Commons, and the Zoology Commons

Makarikov, Arseny A.; Nims, Todd N.; Galbreath, Kurt E.; and Hoberg, Eric P., "Hymenolepis folkertsi n. sp. (Eucestoda: Hymenolepididae) in the Oldfield Mouse Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the Southeastern Nearctic with Comments on Tapeworm Faunal Diversity among Deer Mice" (2015). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 795. http://digitalcommons.unl.edu/parasitologyfacpubs/795

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. This article is a U.S. government work and is not subject to copyright in the United States. Parasitol Res DOI 10.1007/s00436-015-4399-x

ORIGINAL PAPER

Hymenolepis folkertsi n. sp. (Eucestoda: Hymenolepididae) in the oldfield mouse Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the southeastern Nearctic with comments on tapeworm faunal diversity among deer mice

Arseny A. Makarikov & Todd N. Nims & Kurt E. Galbreath & Eric P. Hoberg

Received: 18 December 2014 /Accepted: 27 February 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract A previously unrecognized species of host switching among other cricetid, murid, and geomyid ro- hymenolepidid cestode attributable to Hymenolepis is de- dents in sympatry. scribed based on specimens in Peromyscus polionotus, oldfield mouse, from Georgia near the southeastern coast of Keywords Eucestoda . Hymenolepididae . Hymenolepis continental North America. Specimens of Hymenolepis folkertsi . New species . Morphology . Rodents . Peromyscus folkertsi n. sp. differ from those attributed to most other spe- polionotus . Georgia cies in the genus by having testes arranged in a triangle and a scolex with a prominent rostrum-like protrusion. The newly recognized species is further distinguished by the relative po- sition and length of the cirrus sac, shape of seminal receptacle, and relative size of external seminal vesicle and seminal re- ceptacle. Hymenolepidid cestodes have sporadically been re- Introduction ported among the highly diverse assemblage of Peromyscus which includes 56 distinct species in the Nearctic. Although Muroid rodents of the genus Peromyscus Gloger, 1841 the host genus has a great temporal duration and is endemic to (Cricetidae) are among the most diverse assemblage among the Nearctic, current evidence suggests that tapeworm faunal the Neotominae and represent an endemic complex of 56 spe- diversity reflects relatively recent assembly through bouts of cies occurring with restricted and overlapping distributions across a considerable geographic expanse of North America from near Arctic latitudes into central Mexico (Musser and Carleton 2005). The taxonomy and biogeography of these A. A. Makarikov (*) Institute of Systematics and Ecology of Animals, Siberian Branch of rodents are particularly intricate reflecting both the temporal the Russian Academy of Sciences, Frunze Str. 11, duration of this group with origins in the late Miocene and Novosibirsk, Russia 630091 early Pliocene in the Nearctic and the range of habitats that are e-mail: [email protected] occupied by various species (e.g., Kurtén and Anderson 1980; T. N. Nims Avise et al. 1983;Dragooetal.2006). The extensive geo- Science Department, Georgia Perimeter College, 239 Cedar Lane, graphic range of this assemblage suggests the potential for Covington, GA 30014, USA substantial insights about the history and patterns of North American biogeography and ecology, which can be revealed K. E. Galbreath Department of Biology, Northern Michigan University, 1401 Presque by exploring diversity and faunal assembly of complex host- Isle Ave., Marquette, MI 49855, USA parasite systems (e.g., Whitaker Jr 1968; Whitaker and Hamilton 1998;Hobergetal.2012; Makarikov et al. 2013a). E. P. Hoberg Biodiversity inventory for helminths has involved few spe- United States National Parasite Collection, Animal Parasitic Disease Laboratory, USDA Agricultural Research Service, BARC East No. cies within Peromyscus and has focused, for example, on the 1180, 10300 Baltimore Avenue, Beltsville, MD 20705, USA following: Peromyscus maniculatus (Wagner, 1845) Parasitol Res

(Michigan and Wisconsin—Rausch and Tiner 1949; Pers. Comm.; http://arctos.database.museum/ Quebec—Schad 1954; central plains eastern Rocky SpecimenSearch.cfm). In contrast to the considerable Mountains—Smith 1954; Arizona—Kruidenier and diversity of these neotomine rodents, relatively few Gallicchio 1956; Alberta—Lubinsky 1957;Utah— comprehensive studies of host-parasite diversity have been Grundmann and Frandsen 1960; Colorado and Idaho— conducted and the helminth faunas for most species are Leiby 1961, 1962;Montana—Vaughn 2013), Pe. completely unknown or are based on fragmentary survey data maniculatus, Peromyscus eremicus (Baird, 1857), (e.g., species lists summarized in Erickson 1938;Doran1954; Peromyscus truei (Shufeldt, 1885) and Peromyscus crinitus Whitaker Jr 1968;Dyer1969). (Merriam, 1891) (Nevada—Babero and Matthias 1967), Pe. Although ectoparasites of Peromyscus have been reason- maniculatus and Peromyscus leucopus (Rafinesque, 1818) ably well characterized, there remains minimal information (Illinois—Barker et al. 1987), Peromyscus californicus about helminth diversity in these hosts (Whitaker Jr 1968). (Gambell, 1848), Pe. truei and Peromyscus boylii (Baird, Nematodes are prominent components of most communities 1855) (coastal California—Voge 1952), Pe. boylii and Pe. where data are available, but cestodes appear to be relatively maniculatus (central California—Tinkle 1972)and rare other than species of Catenotaenia Janicki, 1904 and Peromyscus gossypinus (LeConte, 1853), Peromyscus Choanotaenia Railliet, 1896 and may be most often associat- polionotus (Wagner, 1843), and Podomys floridanus ed with other rodent hosts in sympatry (e.g., Erickson 1938; (Chapman, 1889) (Florida—Layne 1963; Kinsella 1991). Smith 1954; Doran 1954; Grundmann and Frandsen 1960; Geographically extensive and often site intensive survey Leiby 1961, 1962;Dyer1969;Barkeretal.1987; Kinsella among species of Peromyscus were conducted by mammalo- 1991)(Table1). For example, hymenolepidids have sporadi- gists associated with the Museum of Southwestern Biology cally been documented among Peromyscus spp. including un- (University of New Mexico) and in the Beringian Coevolution armed cestodes referred to Hymenolepis citelli (McLeod, Project exploring diversity across high latitudes of the 1933) and Hymenolepis diminuta (Rudolphi, 1819) in Pe. Nearctic. In excess of 800 potential hosts were examined in- maniculatus from Utah (Grundmann and Frandsen 1960) cluding Pe. maniculatus, Peromyscus keeni (Rhoads, 1894), and armed Rodentolepis nana (Siebold, 1852) (as and Peromyscus nasutus (Allen, 1891) with cestodes docu- Hymenolepis)inPe. gossypinus, Pe. polionotus,andPo. mented in about 6 % of these rodents (Mariel Campbell, floridanus from Florida (Kinsella 1991). Unidentified

Table 1 Checklist of cestodes reported from Peromyscus spp

Cestode species Host species Locality Reference

Catenotaenia peromysci Smith, 1954 Pe. maniculatus New Mexico, Colorado, Smith (1954) Wyoming, Pe. maniculatus Colorado Leiby (1961) Pe. maniculatus Illinois Barker et al. (1987) Choanotaenia peromysci (Erickson, 1938) Pe. maniculatus Minnesota Erickson (1938) (syn.: Prochoanotaenia peromysci Erickson, 1938) Pe. maniculatus Illinois Barker et al. (1987) Hymenolepis sp. Pe. maniculatus, Pe. eremicus Nevada Babero and Matthias (1967) Pe. maniculatus Minnesota Erickson (1938) Pe. maniculatus Arizona Kruidenier and Gallicchio (1956) Pe. maniculatus Nebraska Hansen (1950) Pe. maniculatus Montana Vaughn (2013) Hymenolepis sp. (cysticercoids) Pe. maniculatus Idaho Leiby (1962) Hymenolepis bennetti Freeman, 1960 Pe. maniculatus Ontario Freeman (1960) Pe. maniculatus, Pe. leucopus Illinois Barker et al. (1987) H. citelli (McLeod, 1933) Pe. maniculatus Utah Grundmann and Frandsen (1960) H. diminuta (Rudolphi, 1819) Pe. maniculatus Utah Grundmann and Frandsen (1960) H. horrida (Linstow, 1901) Pe. truei, Pe. boylii, California Voge (1952) Pe. californicus H. peromysci Tinkle, 1972 Pe. boylii Pe. maniculatus California Tinkle (1972) Rodentolepis nana (Siebold, 1852) Pe. gossypinus, Pe. polionotus Florida Kinsella (1991) (syn.: Hymenolepis nana (Siebold, 1852)) Taenia rileyi Loewen, 1929 (larva) Pe. gossypinus Florida Kinsella (1991) Parasitol Res strobilate specimens of Hymenolepis sp. have been observed investigated hosts are critically important foundations in in Pe. maniculatus and Pe. eremicus from Nevada (Babero broader investigations of faunal diversity and contribute di- and Matthias 1967) and in Pe. maniculatus from Minnesota rectly to empirical assessments of specificity among nominal (Erickson 1938), Arizona (Kruidenier and Gallicchio 1956), taxa. Nebraska (Hansen 1950), and Montana (Vaughn 2013); cys- Our current study establishes a parasitological inventory of ticercoids attributed to Hymenolepis sp. were seen in Pe. Pe. polionotus, or oldfield mouse, from Georgia, USA (Nims maniculatus from Idaho (Leiby 1962). Strobilate specimens et al. 2008; additional data for publication in preparation), a referred to the armed Hymenolepis bennetti Freeman, 1960, species endemic to the southeastern region of North America originally described based on specimens in Napaeozapus occurring from central Tennessee to northern Florida. Prior insignis (Miller, 1891) and Pe. maniculatus from Ontario, records of cestodes in this region are limited to the cosmopol- were also collected in Pe. maniculatus and Pe. leucopus from itan R. nana documented among species of Peromyscus in- Illinois (Freeman 1960; Barker et al. 1987). Another species cluding Pe. polionotus from Florida (Kinsella 1991). Building with an armed scolex, Hymenolepis peromysci Tinkle, 1972, on this current picture of diversity, we now describe and name was described based on specimens in Pe. boylii and also re- a previously unrecognized species of hymenolepidid belong- ported in Pe. maniculatus from central California (Tinkle ing to Hymenolepis (s. str.) Weinland, 1858 which is differen- 1972). Cestodes referred to Hymenolepis horrida (Linstow, tiated from related cestodes based on comparative morpholo- 1901) were examined from Pe. truei, Pe. boylii,andPe. gy. Further, we briefly discuss the biological and historical californicus at localities along coastal California (Voge context for hymenolepidid tapeworm faunas in species of 1952). H. horrida (as Arostrilepis Mas-Coma and Tenora Peromyscus from North America. 1997) is now regarded as a complex of species across the Holarctic, and specimens originally examined by Voge (1952) were recently described as Arostrilepis mariettavogeae Materials and methods Makarikov, Gardner et Hoberg, 2013 in these species of Peromyscus and the heteromyid, Perognathus inornatus Oldfield mice were captured using live traps baited with sun- Merriam, 1889 (Makarikov et al. 2012, 2013a). flower seeds at the Fifteenmile Creek Conservation Easement Over the past century, it was generally accepted that among (32° 21′ 21.8″ N, 82° 01′ 42.4″ W) (The Nature Conservancy mammalian and rodent cestodes, many anoplocephalid, in Georgia), located in Candler County, Georgia, USA, from catenotaeniid, and hymenolepidid species were widespread, November 2002 to February 2003. This location represented a often with intercontinental distributions, and were character- frequently burned (ca. every 3 years) longleaf pine/wiregrass ized by considerable morphological variation without defin- habitat. Captured mice were euthanized in the field with chlo- able limits related either to geography or host association roform. Mammal trapping and euthanasia were carried out (Voge 1952; Schiller 1952; Ryzhikov et al. 1978). Studies using methods recommended by the American Society of across a spectrum of host taxa including rodents have increas- Mammalogists (1998) and approved by Georgia Southern ingly identified the broad occurrence of poorly differentiated University’s Animal Care and Use Committee. Trapping was or cryptic parasite species, suggesting that considerable diver- further authorized by the Georgia Department of Natural sity remains to be discovered and characterized (e.g., Resources (permits 29-WMB-02-83 and 29-WMB-03-105). Haukisalmi et al. 2004, 2010b; Pérez-Ponce de León and Helminths were recovered from small mammals using a Nadler 2010; Makarikov et al. 2013a; Makarikov and Tkach technique described by Pung et al. (2000). The gastrointestinal 2013). Increasing discrimination of species limits and tracts from 30 oldfield mice were examined for helminths. The molecular/morphological partitions among taxa contribute to small intestine and large intestine were each placed in individ- nuanced observations about specificity. Some hymenolepidid ual Petri dishes, covered with water, cut open, and then gently cestodes in rodents appear to maintain specificity to host gen- scraped with insect pins during examination using a dissecting era (Makarikov et al. 2013a, b;MakarikovandTkach2013). microscope (×8 total magnification). Helminths were pre- A similar specificity at the level of host genus was observed served overnight in 5 % formalin and then transferred to among hymenolepidids from various Soricidae (Binkienė 70 % ethanol. et al. 2011). Faunal assembly and specificity are a reflection Cestodes were stained with Ehrlich’s hematoxylin, of historical and microevolutionary processes that have struc- dehydrated in an ethanol series, cleared in clove oil, and tured the biosphere and thus lead to predictions about the mounted in Canada balsam. In the description, measurements distribution of helminth diversity in space and time (e.g., are given in micrometers except where otherwise stated; they Hoberg et al. 2012). Interacting abiotic and biotic mecha- are presented as the range followed by the mean and the num- nisms, and patterns of isolation over time, support the concept ber of the measurements (n) in parentheses. Host taxonomy is that endemic hosts may be predicted to have unique helminth consistent with Wilson and Reeder (2005). The type speci- faunas. Consequently, explorations among poorly mens of the new species have been deposited in the collections Parasitol Res of the Harold W. Manter Laboratory of Parasitology, Description (based on two gravid specimens): Worms of University of Nebraska State Museum, University of medium size. Fully developed strobila 99–116 mm long, with Nebraska-Lincoln, NE, under HWML-75144-75145. maximum width at pregravid or gravid (but not terminal) pro- The following type and voucher materials from previously glottids, 1.71–1.85 mm. Strobila consisting of about 790–850 described species deposited in the United States National craspedote proglottids. Scolex slightly flattened dorsoventral- Parasite Collection, Beltsville, MD (USNPC), were studied ly, 168 wide, clearly distinct from strobila (Fig. 1a). Suckers for comparative analysis: holotype of Hymenolepis unarmed, round or oval, 93–102×70–86 (97×75, n=4), with tualatinensis Gardner, 1985 (USNPC 078418) in the geomyid thick muscular walls, extending beyond lateral margins of Thomomys bulbivorus (Richardson, 1829) from Oregon, ho- scolex. Rhynchus unarmed, 37×4, not fully invaginated in lotype of Hymenolepis pitymi Yarinsky, 1952 (USNPC rostellar pouch and its evaginated part forms rostrum-like pro- 038261) in the arvicoline, Pitymys (= Microtus) pinetorum trusion on apex of scolex; rostellum absent (Fig. 1a). Rostellar (LeConte, 1830) from Tennessee, and a voucher of H. citelli pouch 67×43, with muscular walls, not reaching beyond pos- (USNPC 044825) in the sciurid, Spermophilus terior margins of suckers, osmoregulatory canals penetrate (=Otospermophilus) beecheyi (Richardson, 1829) from through rostellar pouch wall. Neck narrower than scolex, California. Other materials examined by us included tape- 130–145. worms from the collections of Institute of Systematics and Ventral osmoregulatory canals 25–52 (34, n=10) wide, Ecology of Animals, Siberian Branch of the Russian connected by transverse anastomoses. Dorsal osmoregulatory Academy of Sciences, Novosibirsk, representing specimens canals 3–5 (3, n=10) wide, usually situated directly above of H. diminuta in Rattus norvegicus (Berkenhout, 1769) and ventral canals on both sides of proglottids. Genital pores uni- Hymenolepis megaloon Linstow, 1901 in Spermophilus lateral, dextral. Genital ducts pass dorsally to both ventral and undulatus (Pallas, 1778). dorsal longitudinal osmoregulatory canals (Fig. 1c). Development of proglottids gradual, protandrous. External segmentation becomes evident at level of mature part of Results strobila. Mature proglottids 90–150×810–1030 (116×919, n=10), Description transversely elongate, trapezoid (Fig. 1c). Testes relatively small, usually three, almost equal in size, 75–112×44–62 Hymenolepis folkertsi n. sp. (Figs. 1 and 2) (91×52, n=19), oval, normally situated in triangle with flat

Fig. 1 Hymenolepis folkertsi n. sp. a Paratype, dorsoventral view of scolex; b holotype, cirrus and vagina, ventral view; c holotype, hermaphroditic mature proglottids, dorsal view; and d holotype, genital ducts, dorsal view. Scale bars: a, d=100 μm; b=50 μm; and c=300 μm Parasitol Res

Fig. 2 Hymenolepis folkertsi n. sp. a Paratype, pregravid proglottid from ventral side, showing appearance of ventral uterine diverticula (immature eggs are illustrated only on the lateral sides of the uterus); b holotype, gravid proglottid from ventral side, showing saccate uterus with ventral uterine diverticula (mature eggs are illustrated only on the lateral sides of the uterus); c holotype, egg; and d holotype, embryonic hooks. Scale bars: a, b=300 μm; c=20 μm; and d=10 μm

angle; poral testis separated from two antiporal testes by fe- beyond longitudinal osmoregulatory canals (Fig. 2a). With male gonads. Arrangement of testes may vary (triangle with proglottid development, uterus forms numerous diverticula right angle to linear). Cirrus sac pyriform, relatively short, predominantly on ventral side of strobila (Fig. 2b). Testes 138–154×30–39 (145×34, n=14), with thick muscular walls. remain in postmature proglottids; cirrus sac and vagina persist Antiporal part of cirrus sac usually rarely overlapping ventral in pregravid proglottids. Gravid proglottids transversely elon- longitudinal canal but not crossing it (Fig. 1c, d). Genital gate, 230-370×1580-1845 (286×1679, n=15). Fully devel- atrium simple, infundibular, deep, situated approximately in oped uterus occupying entire median field and extending lat- middle or slightly anterior of lateral proglottid margin. Cirrus erally beyond longitudinal osmoregulatory canals, saccate, 45–58×7–10 (51×8, n=15), conical in basal region, fully with ventral and dorsal diverticula, in terminal gravid proglot- evaginated cirrus not available in material examined, armed tids uterine walls indistinguishable (Fig. 2b). Uterus contains with minuscule (less than one long) spines (Fig. 1b). Internal numerous (up to 700–1000) large eggs. Eggs 46–56×57–69 seminal vesicle oval, 78–110×26–33 (92×29, n=13), more (51×61, n=19), subspherical, with relatively thin outer coat than half of cirrus sac length (Fig. 1d). External seminal ves- (up to 1.5), egg surface smooth; oncosphere 22–26×26–35 icle elongate 65–98×31–49 (84×39, n=10), clearly distin- (23×31, n=17) (Fig. 2c). Embryophore subspherical, thin, guishable from vas deferens, distinctly smaller than seminal 23–29×30–39 (25×34, n=18). Embryonic hooks of different receptacle. shape and length (Fig. 2d), antero-lateral embryonic hooks Ovary 147–217 (180, n=10) wide, median, lobed, fan- (16–16.5, n=11) much more robust than slender postero- shaped, ventral to male genital organs, occupying about third lateral (15.7–16.5, n=7) and median hooks (17–18, n=6). of median field width, usually not reaching testes or slightly Taxonomic summary overlapping one of them (Fig. 1c). Vitellarium 30–57×55–98 Site in the host: small intestine. (43×72, n=11), postovarian, median, scarcely lobed. Type host: Pe. polionotus (Wagner, 1843) (Rodentia: Copulatory part of vagina 51–64×4–12 (59×7, n=11), tubu- Cricetidae: Neotominae). lar, with thick walls, clearly distinct from seminal receptacle; Other hosts: currently unknown. ventral to cirrus sac. Vagina surrounded by circular muscula- Type locality: Fifteenmile Creek Conservation Easement ture and covered externally by dense layer of intensely stained (32° 21′ 21.8″ N, 82° 01′ 42.4″ W) (The Nature cells (Fig. 1b). Seminal receptacle relatively large, 275–365× Conservancy in Georgia), Candler County, Georgia, USA. 37–62 (315×49, n=16), elongated, usually curved, or twisted Other localities: currently unknown. (Fig. 1d). Type specimens: holotype, HWML-75144, in type host Uterus first appears as perforated transversely elongated (specimen labeled: ex. Pe. polionotus no. 01-23FEB03-076, sac, situated dorsally to other organs and extending laterally Fifteenmile Creek Conservation Easement (32° 21′ 21.8″ N, Parasitol Res

82° 01′ 42.4″ W) (The Nature Conservancy in Georgia), species C. megalops and Amphipetrovia with type species Candler County, Georgia, USA, 23 February 2003, coll. T. Amphipetrovia biaculeata. Nims). Paratype, HWML-75145, also in type host. Among those species of Hymenolepis in rodents, speci- Symbiotype: skeleton and skin of type host retained and mens of H. folkertsi are readily distinguished by disposition deposited in the Mammalogy collection of the Georgia of the testes arranged in triangle and a scolex with a rostrum- Museum of Natural History, Georgia, USA. like protrusion. In contrast, most congeners in murid, Etymology: this species is named in memory of Dr. George geomyid, spalacid, or sciurid rodents are characterized by a W. Folkerts (1938–2007) in recognition of his significant con- linear arrangement of the testes and a fully invaginated tributions to the knowledge and conservation of native species rhynchus at the apex of the scolex (e.g., in North America: and habitats of the Southeastern USA. H. diminuta, H. citelli,andHymenolepis weldensis Gardner and Schmidt 1988; in the Palearctic including Eurasia: H. diminuta, H. megaloon, Hymenolepis hibernia Remarks Montgomery, Montgomery et Dunn, 1986, and Hymenolepis pseudodiminuta Tenora, Asakawa et Kamiya, 1994, H. folkertsi n. sp. has morphological characters typical of Hymenolepis apodemi Makarikov and Tkach 2013, Hymenolepis (s. str.). Primary diagnostic attributes are a sco- Hymenolepis rymzhanovi Makarikov and Tkach 2013; in lex with rudimentary rostellar apparatus, unarmed rhynchus southern Asia/Philippines: Hymenolepis bicauda Makarikov invaginated in a rostellar pouch, ventral canals with transverse and Tkach 2013, Hymenolepis haukisalmi Makarikov and anastomoses, cirrus sac with muscular walls, vagina Tkach 2013, Hymenolepis bilaterala Makarikov et al. 2015, surrounded by circular musculature, and saccate uterus with and Hymenolepis alterna Makarikov et al. 2015; and in west ventral and dorsal diverticula and spherical eggs (Makarikov Africa: Hymenolepis uranomidis Hunkeler, 1972). and Tkach 2013). Hymenolepis (s. str.) includes about 18 In the Nearctic, cestodes of two species of Hymenolepis nominal taxa occurring among Rodentia in addition to four resemble H. folkertsi in having the testes arranged in a triangle species in Chiroptera and one in Erinaceomorpha (Makarikov and a scolex with a rostrum-like protrusion. These are and Tkach 2013; Makarikov et al. 2013b; Gardner et al. 2014; H. pitymi in the cricetid (Arvicolinae) M. pinetorum (syn.: Makarikov et al. 2015). It should be noted that two species in Pi. pinetorum) from Tennessee (Yarinsky 1952) and birds were attributed to Hymenolepis by Czaplinski and H. tualatinensis in the geomyid T. bulbivorus from western Vaucher (1994). These are Hymenolepis megalops (Nitzsch Oregon (Gardner 1985). H. folkertsi is distinguished from in Creplin, 1829) and Hymenolepis biaculeata Fuhrmann, these species by a larger cirrus sac (138–154, mean 145, ver- 1909. Previously these species had been chosen as the type sus 79 in H. pitymi; 56-150, mean 99 in H. tualatinensis)and species of two independent genera: H. megalops for larger seminal receptacle (275–365×37–62, versus 155–241 Cloacotaenia Wolffhügel, 1938 and H. biaculeata for in H. pitymi;48–169×23–70 in H. tualatinensis). Amphipetrovia Spassky and Spasskaja 1954 (Spassky and Furthermore, the cirrus sac of H. folkertsi rarely overlaps Spasskaja 1954; Spassky 1963). Subsequently, Cloacotaenia and does not cross the ventral longitudinal canal and the ex- and Amphipetrovia were synonymized with Hymenolepis (s. ternal seminal vesicle is distinctly smaller than the seminal l.) by Czaplinski and Vaucher (1994) without any explanation. receptacle. In contrast, the cirrus sac of H. pitymi and However, the morphological characteristics of H. megalops H. tualatinensis substantially crosses the poral osmoregulato- and H. biaculeata significantly differ from species of ry canals and the external seminal vesicle is almost equal in Hymenolepis (s. str.). Among the most remarkable differences length relative to the seminal receptacle. between H. megalops and Hymenolepis (s. str.) may be listed Additionally, in the Nearctic, Hymenolepis robertrauschi the following characters: cirrus sac reaching or crossing mid- Gardner et al. 2014 also superficially resembles H. folkertsi dle line of proglottids vs cirrus sac not reaching middle line of in having testes disposed in a triangle but lacks a rostrum-like proglottids, velum well developed vs velum scarcely devel- protrusion on the scolex. The former species was described in oped or absent, and fully developed uterus compact without grasshopper mice (species of Onychomys Baird, 1858) from pockets and septa not extending laterally beyond longitudinal Nebraska and New Mexico, a cricetid (Neotominae) consid- osmoregulatory canals vs uterus with ventral and dorsal diver- ered to be phylogenetically close to Peromyscus (e.g., Musser ticula extending into both lateral fields. The following features and Carleton 2005; Gardner et al. 2014). Consequently, we distinguish H. biaculeata and Hymenolepis (s. str.): female consider that it is necessary to distinguish these two conge- gonads shifted to poral side of proglottids and testes not sep- ners. H. folkertsi can be differentiated from H. robertrauschi arated by ovary vs median female gonads and testes separated by a smaller scolex (168 versus 199-257) and suckers (93– by ovary (see Spassky and Spasskaja 1954; Spassky 1963; 102×70–86 versus 119-164×82-95), shorter cirrus sac (138– Makarikov and Tkach 2013). In view of this, we are restoring 154, mean 145 versus 147–233, mean 193), cirrus spination independent status of the genera Cloacotaenia with type (length of spines less than 1 versus 1.3), and a larger seminal Parasitol Res receptacle (275–365×37–62 versus 190-246×45-121). canals penetrate through the walls of the rostellar pouch rather Furthermore, the external seminal vesicle in H. folkertsi is than into the rostellum. distinctly smaller than the seminal receptacle, whereas these The microanatomic structure and functional significance of structures are almost equal in length in specimens of a rudimentary rostellar apparatus were well studied in the type H. robertrauschi (see Gardner et al. 2014). species, H. diminuta. Wardle and McLeod (1952) postulated A representative series of voucher specimens of that the unarmed rostellum may serve as an apical sucker, hymenolepidid cestodes from prior studies of Peromyscus helping in fixation to the host intestine. Such an assumption, spp. were not available for comparison, and strobilate cestodes however, was not supported due to the poor muscular devel- were apparently not deposited following many surveys in- opment of the rudimentary rostellar apparatus in H. diminuta volving this assemblage of rodent species across North (Specian and Lumsden 1980). The presence of numerous sen- America (e.g., Erickson 1938;Hansen1950; Grundmann silla in the tegument of the apical organ of H. diminuta sug- and Frandsen 1960; Babero and Matthias 1967; Vaughn gested a sensory function (Specian and Lumsden 1980). In 2013). Access to new comparative materials for concurrent addition, glandular cells or tissue in the rostellar pouch indi- or integrated morphological/molecular analyses is essential cates an excretory/secretory role for this organ. Secretions are to enhance our ability to more completely document parasite released from the apex of the apical invagination (rhynchus) at faunal diversity among Peromyscus spp. and other rodents the mucosal interface in the host intestine, although the func- (e.g., Haukisalmi et al. 2010a; Makarikov et al. 2013a, b). tion for materials secreted from the gland cells remains uncer- Deposition of specimens from inventories is a basic founda- tain (Specian and Lumsden 1980, 1981). Secretory activity tion for characterization of faunal structure (e.g., Hoberg et al. associated with the glands of the rostellar pouch may be in- 2009) and is increasingly necessary given the expanding rec- volved in avoidance of host immune responses targeted to- ognition of cryptic diversity across many groups of parasites ward tapeworms localized in the mucosa, though this requires and hosts (Pérez-Ponce de León and Nadler 2010). further study (Pospekhova 2009). The function of a modified and rudimentary rostellar appa- ratus of H. folkertsi (i.e., appearance of rostrum-like protru- sion), and other species where this structure has been docu- Discussion mented, remains to be determined. We suggest that the partic- ular shape of the scolex may facilitate penetration into spaces H. folkertsi n. sp. is described based on specimens in the among the intestinal villi leading to better adhesion and main- oldfield mouse collected from central Georgia. As such, these tenance of position in the host intestinal tract. This would not tapeworms represent the first species of Hymenolepis (s. str.) exclude the possibility that the rostrum-like protrusion has a to be formally described from the large assemblage of sensory function or that it could serve a role in release of Peromyscus species from North America. Discovery and char- cellular secretions. acterization of these cestodes afford the opportunity to discuss some anatomical characters typical among species of Phylogeny Hymenolepis (s. str.). Further, we explore our current under- standing of hymenolepidid faunas documented among Spassky (1992) considered hymenolepidids with an unarmed Peromyscus relative to patterns of host biogeography and di- scolex parasitizing mammalian hosts to be paraphyletic. versity in North America. Recent molecular phylogenetic studies (Haukisalmi et al. 2010a;GreimanandTkach2012)havecorroboratedthishy- Scolex anatomy and function pothesis and have demonstrated that the loss of the rostellum, or the rostellar armature, has occurred in several independent The rostellar hooks and rostellum are secondarily reduced lineages of hymenolepidids among mammals. For example, among species of Hymenolepis (s. str.). However, the rudi- this is exemplified by species of the Arostrilepis horrida com- mentary rostellar apparatus is conserved. A uniform anatomy plex (syn.: Hymenolepis horrida), which are not closely relat- of the rostellar apparatus can be recognized among all known ed to Hymenolepis (Haukisalmi et al. 2010a), yet they lack a species of the genus, consisting of an unarmed rhynchus in- rostellum. vaginated in the muscular-walled rostellar pouch (Makarikov Following numerous revisions, the genus Hymenolepis (s. and Tkach 2013). Thus, we consider that the apical organ of str.) currently represents a morphologically homogenous and Hymenolepis species described in some publications as a ros- probably monophyletic group (see the generic diagnosis of tellum is homologous with the rostellar pouch (Yarinsky Hymenolepis (s. str.) sensu Makarikov and Tkach 2013). 1952; Singh 1956;Arai1980;Mas-ComaandTenora1997). However, the taxonomic significance of some morphological This hypothesis is further supported by the observation that characters in this genus is not fully determined. Gulyaev and among mammalian hymenolepidids, the osmoregulatory Mel’nikova (2005) considered differences in the cirrus sac Parasitol Res wall structure (absence or presence of distinct muscular walls tapeworms, including some with obvious cosmopolitan distri- of the cirrus sac) and relative position of dorsal and ventral butions due to anthropogenic or natural introduction and in- osmoregulatory canals to be characters of generic level in this vasion (i.e., H. citelli, H. diminuta, A. horrida (s. l.), and group. For example, there are four species of Hymenolepis in R. nana). In contrast, only five species of tapeworms have murid rodents from the Philippines, each of which have a been described as specific parasites of deer mice, associated unique relative positioning of the dorsal and ventral osmoreg- with Pe. boylii, Pe. leucopus,andPe. maniculatus (i.e., ulatory canals and a cirrus sac wall with different thickness. If H. peromysci, H. bennetti, A. mariettavogeae, Choanotaenia one accepts the generic-level characters proposed by Gulyaev peromysci (Erickson 1938)(syn.:Prochoanotaenia peromysci and Mel’nikova (2005), all four species from the Philippines Erickson, 1938), and C. peromysci Smith, 1954). Such a small should be placed in four new genera because each of them has number of apparently host-specific and phylogenetically dis- a unique combination of these features (Makarikov et al. parate cestodes in Peromyscus species may indicate relatively 2013b, 2015). However, due to the lack of detailed phyloge- recent assembly of tapeworm faunas in these Nearctic rodents. netic studies within this lineage of mammalian These faunas contrast with the diverse hymenolepidids, hymenolepidids, we refrain from further generic splitting of anoplocephalids, and catenotaeniids among Arvicolinae, the Hymenolepis. Future phylogenetic studies incorporating a Neotominae, and other rodents across the Holarctic region greater number of Hymenolepis species from different hosts (e.g., Haukisalmi et al. 2010b; Makarikov et al. 2013a; will allow us to better understand the evolution of this globally Haukisalmi et al. 2014). Conversely, our initial impression distributed lineage of hymenolepidid cestodes and to reevalu- of a depauperate cestode fauna may reflect limited study of ate the morphological characters currently used in their sys- host species. We assume that a more comprehensive survey tematic arrangement (Tkach et al. unpublished observation). and inventory of the intestinal helminths among species of Peromyscus and a diverse assemblage of other temperate lat- Hymenolepidid diversity among rodents itude rodents in the Nearctic will result in the discovery of additional previously unknown cestodes. Such a survey must Hymenolepidids among rodents constitute an assemblage of be both geographically widespread and site intensive to ensure genera and species (e.g., Ryzhikov et al. 1978) that occur that parasite diversity is thoroughly documented. In the cur- across all continents except Antarctica and are broadly but rent study, only one of 30 Pe. polionotus was infected with unevenly represented among cricetids, geomyids, specimens of H. folkertsi. Such low prevalence highlights the heteromyids, murids, sciurids, spalacids, glirids, and dipodids. need for sampling efforts to be extensive. Diversity of Hymenolepis (s. str.) among rodent hosts includ- Although the host genus has a relatively deep history and is ing H. folkertsi now includes about 19 species. These cestodes endemic to the Nearctic, current evidence suggests that tape- are globally distributed as parasites in at least five families of worm faunal diversity reflects relatively recent bouts of host Rodentia (i.e., Muridae, Geomyidae, Sciuridae, Cricetidae, switching from sympatric geomyid, murine, neotomine, and and Spalacidae) (Gardner and Schmidt 1988; Makarikov and arvicoline rodents, rather than deep ancestral host-parasite as- Tkach 2013; Makarikov et al. 2013b; Gardner et al. 2014; sociations. Among Muroidea, rodents unequivocally recog- Makarikov et al. 2015). Geographic and host distribution sug- nized as Peromyscus appear in North America during the gests that diversification among species of Hymenolepis has Miocene, with some extant species present by the been linked to colonization of unrelated taxa of Muroidea and Pleistocene (Kurtén and Anderson 1980; Musser and other Rodentia during the process of host radiation. Carleton 2005). Extensive diversification among species of Furthermore, ecological similarity of some rodents, chirop- Peromyscus occurred over the past 2 million years under ep- terans, and soricomorphs is consistent with the possibility of isodes of habitat fragmentation linked to glacial-interglacial mutual exchanges of these helminths between phylogenetical- cycles and shifting climate during the Quaternary (e.g., ly distinct groups of small mammals, supporting current ideas Avise et al. 1983; Dragoo et al. 2006). The late Pliocene and about the importance of host switching and ecological fitting Quaternary also coincided with considerable development and in diversification of complex faunas (e.g., Hoberg and Brooks diversification of rodent faunas with temporally circumscribed 2008;Agostaetal.2010; Brooks et al. 2014). episodes of expansion out of Eurasia into North America The diversity (56 species in the Nearctic; Musser and (Repenning 2001;Hopeetal.2013). Episodic faunal mixing, Carleton 2005), ecological distinctiveness (Nowak 1999), cyclic isolation, and expansion may be reflected in the overall and deep phylogenetic distance (Steppan et al. 2004)between diversity of cestode faunas, assembled from multiple and dis- Peromyscus and other rodent genera suggest that these rodents parate sources, and in the relatively depauperate and hetero- could have a deep association with a unique cestode fauna. geneous distributions that are now observed for However, hymenolepidid cestodes have only sporadically hymenolepidids and other taxa among species of Peromyscus. been reported from Peromyscus, and those that are most often Faunal assembly involving temporal and geographic mo- documented from these mice tend to be widespread species of saics related to recurrent events of geographic expansion and Parasitol Res contact among potential host groups and host switching ap- Arai H (1980) Biology of the Tapeworm Hymenolepis diminuta.New pear to be important drivers in establishing regional assem- York Academic Press, New York Avise JC, Shapira JF, Daniel SW, Aquadro CF, Lansman RA (1983) blages of cestodes among rodents (e.g., Haukisalmi et al. Mitochondrial DNA differentiation during the speciation process 2010b; Hoberg et al. 2012; Makarikov et al. 2012). For exam- in Peromyscus. Mol Biol Evol 1:38–56 ple, among hymenolepidids, the genus Arostrilepis appears to Babero BB, Matthias D (1967) Protospirura peromysci n. sp. (Nematoda: be the sister of tapeworms among Soricomorpha with origins Spiruridea) and other helminths from Peromyscus spp. in Nevada. Proc Helminthol Soc Wash 34:255–261 then attributable to host colonization of Arvicolinae (e.g., Barker CM, Dyer WG, Feldhamer GA (1987) Helminths of Peromyscus Haukisalmi et al. 2010a); subsequent diversification reflects leucopus, P. maniculatus and Blarina carolinensis from southern episodes of host colonization among geomyid and neotomine Illinois. Trans Ill Acad Sci 80:119–127 rodents (e.g., Makarikov et al. 2012; Hoberg et al. 2012). Binkienė R, Kontrimavichus V, Hoberg EP (2011) Overview of the ces- Considering H. folkertsi, morphological similarity among tode fauna of European shrews of the genus Sorex with comments on the fauna in Neomys and Crocidura and an exploration of histor- Nearctic species is observed for H. tualatinensis in a geomyid ical processes in post-glacial Europe. Helminthologia 48:207–228. from central Oregon, H. pitymi in an arvicoline from doi:10.2478/s11687-011-0031-5 Tennessee, and H. robertrauschi in species of Onychomys a Brooks DR, Hoberg EP,Boeger WA, Gardner SL, Galbreath KE, Herczeg related neotomine, and putative sister of Peromyscus,across D, Mejía-Madrid HH, Rácz SE, Dursahinhan AT (2014) Finding them before they find us: informatics, parasites, and environments west-central North America from southern Canada to northern in accelerating climate change. Comp Parasitol 81:155–164. doi:10. Mexico. Extensive sampling and inventory of rodent faunas 1654/4724b.1 and a phylogenetic context for cestodes will contribute to Doran DJ (1954) A catalogue of the Protozoa and helminths of North evaluation of hypotheses for intricate histories of host and American rodents. II. Cestoda. Am Midl Nat 52:469–480 parasite association and regional faunal development over Dragoo JW, Lackey JA, Moore KE, Lessa EP, Cook JA, Yates TL (2006) Phylogeography of the deer mouse (Peromyscus maniculatus) pro- time. vides a predictive framework for research on hantaviruses. J Gen Virol 87:1997–2003. doi:10.1099/vir. 0.81576-0 Acknowledgments We thank Dr. Jean Mariaux (Natural History Mu- Dyer WG (1969) A checklist of the Protozoa and helminths of the deer seum, Geneva, Switzerland), Dr. Patricia Pilitt (US National Parasite Col- mouse Peromyscus maniculatus in North America. Am Midl Nat lection, Beltsville, MD, USA), and Dr. Scott L. Gardner (Harold W. 81:258–262 Manter Laboratory of Parasitology, Lincoln, NE, USA), for specimen Erickson AB (1938) Parasites of some Minnesota Cricetidae and loans and/or providing conditions and laboratory space for examination Zapodidae, and a host catalogue of helminth parasites of native of the type and voucher specimens. We thank Dr. Oscar Pung (Georgia American mice. Am Midl Nat 20:575–589 Southern University (GSU), Statesboro, GA, USA) for his assistance with Freeman RS (1960) Another hymenolepidid with great morphological the mouse dissections. We thank The Nature Conservancy in Georgia for variation, Hymenolepis bennetti n. sp. (Cestoda) from allowing access to their managed lands. We are grateful for access to the Napaeozapus insignis algonquinensis Prince. Can J Zool 38:737– Arctos database through the Museum of Southwestern Biology, Univer- 743 sity of New Mexico, and a summary of inventory for parasites in species Gardner SL (1985) Helminth parasites of Thomomys bulbivorus of Peromyscus prepared by Mariel Campbell. We sincerely thank Dr. (Richardson) (Rodentia: Geomyidae), with the description of a Scott L. Gardner and an anonymous reviewer for their detailed comments new species of Hymenolepis (Cestoda). Can J Zool 63:1463–1469 that improved our manuscript. Research by AAM was supported in part Gardner SL, Schmidt GD (1988) Cestodes of the genus Hymenolepis by the Russian Fund for Fundamental Research (Project No. 14-04- Weinland, 1858 sensu stricto from pocket gophers Geomys and 00871-a). Further support for AAM was provided by the National Sci- Thomomys spp. (Rodentia: Geomyidae) in Colorado and Oregon, ence Foundation (DEB 0819696 and 0818823) through grants addressing with a discriminant analysis of four species of Hymenolepis.CanJ cestode diversity coordinated by Dr. Janine Caira, University of Connect- Zool 66:896–903 icut. This is also a contribution to understanding history and diversity of Gardner SL, Luedders BA, Duszynski DW (2014) Hymenolepis mammalian helminth faunas supported by NSF through the Beringian robertrauschi n. sp. from grasshopper mice Onychomys spp. in Coevolution Project (DEB 0196095 and 0415668) and the Integrated New Mexico and Nebraska, U.S.A. Occas Pap Mus Texas Tech Inventory of Biomes of the Arctic (DEB-Biodiversity Discovery and Univ 322:1–10 Analysis-1258010) to J.A. Cook (University of New Mexico), EPH, Greiman SE, Tkach VV (2012) Description and phylogenetic relation- and KEG. 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